Mechanisms of Memory Enhancement
Keywords:
memory enhancement, learning and memory, animal models
Abstract
The ongoing quest for memory enhancement is one that grows necessary as the global population increasingly ages. The extraordinary progress that has been made in the past few decades elucidating the underlying mechanisms of how long-term memories are formed has provided insight into how memories might also be enhanced. Capitalizing on this knowledge, it has been postulated that targeting many of the same mechanisms, including CREB activation, AMPA/ NMDA receptor trafficking, neuromodulation (e.g. via dopamine, adrenaline, cortisol or acetylcholine) and metabolic processes (e.g. via glucose and insulin) may all lead to the enhancement of memory. These and other mechanisms and/or approaches have been tested via genetic or pharmacological methods in animal models, and several have been investigated in humans as well. In addition, a number of behavioral methods, including exercise and reconsolidation, may also serve to strengthen and enhance memories. By capitalizing on this knowledge and continuing to investigate these promising avenues, memory enhancement may indeed be achieved in the future.
Downloads
Download data is not yet available.
References
[76] Advokat, C. (2010). What are the cognitive effects of stimulant medications? Emphasis on adults with attention-deficit/hyperactivity disorder (ADHD). Neuroscience and biobehavioral reviews, 34: 1256–1266.
[89] Agis-Balboa, R. C., Arcos-Diaz, D., Wittnam, J., Govindarajan, N., Blom, K., Burkhardt, S., Haladyniak, U., Agbemenyah, H. Y., Zovoilis, A., Salinas-Riester, G., et al. (2011). A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. The EMBO journal, 30: 4071–4083.
[22] Alberini, C. M. (2008). The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol Learn Mem, 89: 234–246.
[1] Alberini, C. M. (2009). Transcription Factors in Long-Term Memory and Synaptic Plasticity. Physiolological Reviews, 89: 121–145.
[28] Alberini, C. M. (2012). Chen DY. Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends in neurosciences, 35: 274–283.
[97] Alberini, C. M., Milekic, M. H., Tronel, S. (2006). Mechanisms of memory stabilization and de-stabilization. Cellular and molecular life sciences, 63: 999–1008.
[81] Azari, N. P. (1991). Psychopharmacology Effects of glucose on memory processes in young adults. Psychopharmacology, 105: 521–524.
[37] Barco, A., Pittenger, C., Kandel, E. R. (2003). CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert opinion on therapeutic targets, 7: 101–114.
[24] Bartsch, D., Ghirardi, M., Skehel, P.A., Karl, K. A., Herder, S. P., Chen, M., Bailey, C. H., Kandel, E. R. (1995). Aplysia CREB2 Represses Long-Term Facilitation: Relief of Repression Converts Transient Facilitation into Long-Term Functional and Structural Change. Cell, 83: 979–992.
[95] Bekinschtein, P., Cammarota, M., Igaz, L. M., Bevilaqua, L. R., Izquierdo, I., Medina, J. H. (2007). Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus. Neuron, 53: 261–277.
[86] Benedict, C., Hallschmid, M., Hatke, A., Schultes, B., Fehm, H. L., Born, J., Kern, W. (2004). Intranasal insulin improves memory in humans. Psychoneuroendocrinology, 29: 1326–1334.
[78] Birks, J. (2009). Cholinesterase inhibitors for Alzheimer’s disease (Review). The Cochrane Library.
[2] Bliss, T. V. P., Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361: 31–39.
[60] Bourne, J., Harris, K. M. (2007). Do thin spines learn to be mushroom spines that remember? Current opinion in neurobiology, 17: 381–386.
[27] Brightwell, J. J., Smith, Ca., Neve, R. L., Colombo, P. J. (2007). Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learning &memory, 14: 195–199.
[45] Burgdorf, J., Zhang, X.-l., Weiss, C., Matthews, E., Disterhoft, J. F., Stanton, P. K., Moskal, J. R. (2011). The Nmethyl-D-aspartate receptor modulator GLYX-13 enhances learning and memory in young adult and learning impaired aged rats. Neurobiology of aging, 21: 698–706.
[59] Cambon, K., Hansen, S. M., Venero, C., Herrero, aI., Skibo, G., Berezin, V., Bock, E., Sandi, C. (2004). A synthetic neural cell adhesion molecule mimetic peptide promotes synaptogenesis, enhances presynaptic function, and facilitates memory consolidation. The Journal of neuroscience, 24: 4197–4204.
[15] Cansino, S. (2009). Episodic memory decay along the adult lifespan: a review of behavioral and neurophysiological evidence. Int J Psychophysiol, 71: 64–69.
[12] Carlesimo, G. A, Oscar-Berman, M. (1992). Memory deficits in Alzheimer's patients: a comprehensive review. Neuropsychol Rev, 3: 119–169.
[65] Castner, Sa., Goldman-Rakic, P. S. (2004). Enhancement of working memory in aged monkeys by a sensitizing regimen of dopamine D1 receptor stimulation. The Journal of neuroscience, 24: 1446–1450.
[30] Chen, A., Muzzio, Ia., Malleret, G., Bartsch, D., Verbitsky, M., Pavlidis, P., Yonan, A. L., Vronskaya, S., Grody, M. B., Cepeda, I., et al. (2003). Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins. Neuron, 39: 655–669.
[36] Chen, D. Y., Stern, Sa., Garcia-Osta, A., Saunier-Rebori, B., Pollonini, G., Bambah-Mukku, D., Blitzer, R. D., Alberini, C. M. (2011). A critical role for IGF-II in memory consolidation and enhancement. Nature, 469: 491–497.
[5] Cooke, S. F, Bliss, T. V. P. (2003). Cellular and Molecular Life Sciences Visions & Reflections The genetic enhancement of memory. Neuropharmacology, 60: 1–5.
[18] Corkin, S, Amaral, D. G., Gonzalez, R. G., Johnson, K. A. (1997). Hyman BTHM's medial temporal lobe lesion: findings from magnetic resonance imaging. J Neurosci, 17: 3964–3979.
[7] Cowan, N. (2008). What are the differences between long-term, short-term, and working memory? Prog Brain Res, 169: 323–338.
[87] Craft, S., Asthana, S., Newcomer, J. W., Wilkinson, C. W., Matos, I. T., Baker, L. D., Cherrier, M., Lofgreen, C., Latendresse, S., Petrova, A., et al. (1999). Enhancement of memory in Alzheimer disease with insulin and somatostatin, but not glucose. Archives of general psychiatry, 56: 1135–1140.
[88] Craft, S., Baker, L. D., Montine, T. J., Minoshima, S., Watson, G. S., Claxton, A., Arbuckle, M., Callaghan, M., Tsai, E., Plymate, S. R., et al. (2012). Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Archives of neurology, 69: 29–38.
[40] Cui, Y., Jin, J., Zhang, X., Xu, H., Yang, L., Du, D., Zeng, Q., Tsien, J. Z., Yu, H., Cao, X. (2011). Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PloS one, 6: e20312.
[42] Danysz, W., Zajaczkowski, W., Parsons, C. G. (1995). Modulation of leaning processes by ionotropic glutamate receptor ligands. Behavioral Pharmacology, 6: 455–474.
[20] Davis, H. P, Squire, L. R. (1984). Protein synthesis and memory: a review. Psychological bulletin, 96: 518–559.
[100] Dębiec, J., Bush, DEa., LeDoux, J. E. (2011). Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats--a possible mechanism for the persistence of traumatic memories in PTSD. Depression and anxiety, 28: 186–193.
[77] Deiana, S., Platt, B., Riedel, G. (2011). The cholinergic system and spatial learning. Behavioural brain research, 221: 389–411.
[67] de Lima, M. N. M., Presti-Torres, J., Dornelles, A., Scalco, F. S., Roesler, R., Garcia, V. A., Schröder, N. (2011). Modulatory influence of dopamine receptors on consolidation of object recognition memory. Neurobiology of learning and memory, 95: 305–310.
[58] Diana, G., Valentini, G., Travaglione, S., Falzano, L., Pieri, M., Zona, C., Meschini, S., Fabbri, A., Fiorentini, C. (2007). Enhancement of learning and memory after activation of cerebral Rho GTPases. Proceedings of the National Academy of Sciences, 104: 636–641.
[14] Dubois, B., Pillon, B. (1997). Cognitive deficits in Parkinson’s disease. Journal of Neurology, 244: 2–8.
[6] Ebbinghaus, H. (1913). Memory: A contribution to experimental psychology. Teachers College, Columbia University.
[51] Ehlers, M. D. (2000). Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron, 28: 511–525.
[71] Eich, T. S., Metcalfe, J. (2009). Effects of the stress of marathon running on implicit and explicit memory. Psychonomic bulletin & review, 16: 475–479.
[62] Floresco, S. B. (2011), Jentsch JD. Pharmacological enhancement of memory and executive functioning in laboratory animals. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology, 36: 227–250.
[82] Foster, J. K., Lidder, P. G., Sünram, S. I. (1998) Glucose and memory: fractionation of enhancement effects? Psychopharmacology, 137: 259–270.
[73] Gold, P. E., Ruskirk, R. V. A. N. (1976). Effects of Posttrial Hormone Injections on Memory Processed. Hormones and Behavior, 7: 509–517.
[84] Gold, P. E., Vogt, J., Hall, J. L. (1986). Glucose effects on memory: behavioral and pharmacological characteristics. Behavioral and neural biology, 46: 145–155.
[91] Hawkes, C., Jhamandas, J. H., Harris, K. H., Fu, W., MacDonald, R. G., Kar, S. (2006). Single transmembrane domain insulin-like growth factor-II/mannose-6-phosphate receptor regulates central cholinergic function by activating a G-protein-sensitive, protein kinase C-dependent pathway. The Journal of neuroscience: the official journal of the Society for Neuroscience, 26: 585–596.
[66] Haycock, J. W., Van Buskirk, R., Ryan, J. R., McGaugh, J. L. (1977). Enhancement of retention with centrally administered catecholamines. Experimental neurology, 54: 199–208.
[54] Hu, H., Real, E., Takamiya, K., Kang, M.-G., Ledoux, J., Huganir, R. L., Malinow, R. (2007). Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell, 131: 160–173.
[99] Inda, M. C., Muravieva, E. V., Alberini, C. M. (2011). Memory retrieval and the passage of time: from reconsolidation and strengthening to extinction. The Journal of neuroscience: the official journal of the Society for Neuroscience, 31: 1635–1643.
[43] Izquierdo, I. (1994). Pharmacological in memory evidence for a role of long-term potentiation. The FASEB Journal, 8: 1139–1145.
[26] Josselyn, Sa., Shi, C., Carlezon, Wa, Neve, R. L., Nestler, E. J., Davis, M. (2001). Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. The Journal of neuroscience, 21: 2404–2412.
[46] Kalisch, R., Holt, B., Petrovic, P., De Martino, B., Klöppel, S., Büchel, C., Dolan, R. J. (2009). The NMDA agonist D-cycloserine facilitates fear memory consolidation in humans. Cerebral cortex, 19: 187–196.
[55] Krugers, H. J., Hoogenraad, C. C., Groc, L. (2010). Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nature reviews. Neuroscience, 11: 675–681.
[61] Kupfermann, I. (1979). Modulatory actions of neurotransmitters. Annual review of neuroscience, 2: 447–465.
[38] Lamprecht, R., LeDoux, J. (2004). Structural plasticity and memory. Nature reviews. Neuroscience, 5: 45–54.
[80] Lapp, J. E. (1981). Effects of Glycemic Alterations and Noun Imagery on the Learning of Paired Associates. Journal of Learning Disabilities, 14: 35–38.
[29] Lee, J.-A., Kim, H., Kim, K., Han, J. (2001). Overexpression of and RNA interference with the CCAAT enhancer-binding protein on long-term facilitation of Aplysia sensory to motor synapses. Learning and Memory, 8: 220–226.
[4] Lee, Y-S, Silva, A. J. (2009). The molecular and cellular biology of enhanced cognition. Nature reviews. Neuroscience, 10: 126–140.
[102] Leuner, B., Shors, T. J. (2004). New spines, new memories. Mol Neurobiol, 29: 117–130.
[16] Light, L. L. (1991). Memory and aging: four hypotheses in search of data. Annu Rev Psychol, 42: 333–376.
[75] Linssen, aM. W., Vuurman, E. F. P. M., Sambeth, A., Riedel, W. J. (2011). Methylphenidate produces selective enhancement of declarative memory consolidation in healthy volunteers. Psychopharmacology.
[93] Lynch, G. (2002). Memory enhancement: the search for mechanism-based drugs. Nature neuroscience, 5(Suppl): 1035–1038.
[52] Lynch, G. (2006). Glutamate-based therapeutic approaches: ampakines. Current opinion in pharmacology, 6: 82–88.
[10] Lynch, G, Palmer, L.C., Gall, C. M. (2011). The likelihood of cognitive enhancement. Pharmacology, biochemistry, and behavior, 99: 116–129.
[33] Malleret, G., Haditsch, U., Genoux, D., Jones, M. W., Bliss, T. V., Vanhoose, aM., Weitlauf, C., Kandel, E. R., Winder, D. G., Mansuy, I. M. (2001). Inducible and reversible enhancement of learning, memory, and longterm potentiation by genetic inhibition of calcineurin. Cell, 104: 675–686.
[8] McGaugh, J. L. (2000). Memory - A Century of Consolidation. Science, 287: 248–251.
[9] Nader, K, Einarsson, E. O. (2010). Memory reconsolidation: an update. Ann N Y Acad Sci, 1191: 27–41.
[69] McGaugh, J. L., Roozendaal, B. (2002). Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology, 12: 205–210.
[63] Mckeith, I. G., Burn, D. (2000). Spectrum of Parkinson's Disease, Parkinson's Dementia, and Lewy Body Dementia. Neurologic Clinics, 18: 865–883.
[85] McNay, E. C., Ong, C. T., McCrimmon, R. J., Cresswell, J., Bogan, J. S., Sherwin, R. S. (2010). Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiology of learning and memory, 93: 546–553.
[56] McReynolds, J. R., Donowho, K., Abdi, A., McGaugh, J. L., Roozendaal, B., McIntyre, C.K. (2010). Memoryenhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiology of learning and memory, 93: 312–321.
[49] Migues, P. V., Hardt, O., Wu, D. C., Gamache, K., Sacktor, T. C., Wang, Y. T., Nader, K. (2010). PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nature neuroscience, 13: 630–634.
[103] Mizuno, K., Giese, K. P. (2010). Towards a molecular understanding of sex differences in memory formation. Trends Neurosci, 33: 285–291.
[57] Okuno, H., Akashi, K., Ishii, Y., Yagishita-Kyo, N., Suzuki, K., Nonaka, M., Kawashima, T., Fujii, H., Takemoto-Kimura, S., Abe, M., et al. (2012). Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIbeta. Cell, 149: 886–898.
[13] Perry, R. J., Hodges, J. R. (1999). Attention and executive deficits in Alzheimer’s disease A critical review. Brain, 122: 383–404.
[96] Pinsker, H. M, Hening, W. A., Carew, T. J., Kandel, E. R. (1973). Long-term sensitization of a defensive withdrawal reflex in Aplysia. Science, 182: 1039–1042.
[79] Prickaerts, J., Sik, A., van der Staay, F. J., de Vente, J., Blokland, A. (2005). Dissociable effects of acetylcholinesterase inhibitors and phosphodiesterase type 5 inhibitors on object recognition memory: acquisition versus consolidation. Psychopharmacology, 177: 381–390.
[48] Rao, V. R., Finkbeiner, S. (2007). NMDA and AMPA receptors: old channels, new tricks. Trends in Neurosciences, 30: 284–291.
[92] Reinhardt, R. R., Bondy, C. A. (1994). Insulin-Like Growth Factors Cross the Blood-Brain Barrier. Endocrinology, 135: 1753–1761.
[3] Ressler, K. J., Mayberg, H. S. (2007). Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nature neuroscience, 10: 1116–1124.
[41] Riedel, G., Platt, B., Micheau, J. (2003). Glutamate receptor function in learning and memory. Behavioural brain research, 140: 1–47.
[74] Roozendaal, B., Nguyen, B. T., Power, A. E., Mcgaugh, J. L. (1999). Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proceedings of the National Academy of Sciences, 96: 11642–11647.
[72] Roozendaal, B., Okuda, S., Van der Zee, Ea., McGaugh, J.L. (2006). Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences, 103: 6741–6746.
[90] Roth, Ra. (1988). Structure of the receptor for insulin-like growth factor II: the puzzle amplified. Science, 239: 1269–1271.
[98] Sara, S. J. (2000). Strengthening the shaky trace through retrieval. Nature reviews. Neuroscience, 1: 212–213.
[34] Sharma, S. K., Bagnall, M. W., Sutton, Ma., Carew, T. J. (2003). Inhibition of calcineurin facilitates the induction of memory for sensitization in Aplysia: requirement of mitogen-activated protein kinase. Proceedings of the National Academy of Sciences of the United States of America, 100: 4861–4866.
[23] Sharma, A. V., Nargang, F. E., Dickson, C.T. (2012). Neurosilence: profound suppression of neural activity following intracerebral administration of the protein synthesis inhibitor anisomycin. J Neurosci, 32: 2377–2387.
[50] Shema, R., Haramati, S., Ron, S., Hazvi, S., Chen, A., Sacktor, T. C., Dudai, Y. (2011). Enhancement of consolidated long-term memory by overexpression of protein kinase Mzeta in the neocortex. Science, 331: 1207–1210.
[11] Simard, M, Reekum, R. V. (1999). Memory Assessment in Studies of Cognition-Enhancing Drugs for Alzheimer’s Disease. Drugs and Aging, 14: 197–230.
[53] Slutsky, I., Abumaria, N., Wu, L.-J., Huang, C., Zhang, L., Li, B., Zhao, X., Govindarajan, A., Zhao, M.-G., Zhuo, M., et al. (2010). Enhancement of learning and memory by elevating brain magnesium. Neuron, 65: 165–177.
[83] Smith, Ma, Riby, L. M., Eekelen, J. A. M. V., Foster, J. K. (2011). Glucose enhancement of human memory: a comprehensive research review of the glucose memory facilitation effect. Neuroscience and biobehavioral reviews, 35: 770–783.
[17] Squire, L. R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological review, 99: 195–231.
[39] Tang, Y. P., Shimizu, E., Dube, G. R., Rampon, C., Kerchner, Ga., Zhuo, M., Liu, G., Tsien, J. Z. (1999). Genetic enhancement of learning and memory in mice. Nature, 401: 63–69.
[101] Tian, S., Huang, F., Li, P., Li, Z., Zhou, S., Deng, H., Yang, Y. (2011). Nicotine enhances contextual fear memory reconsolidation in rats. Neuroscience letters, 487: 368–371.
[35] Tully, T., Bourtchouladze, R., Scott, R., Tallman, J. (2003). Targeting the CREB pathway for memory enhancers. Nature reviews. Drug discovery, 2: 267–277.
[94] van Praag, H. (2009). Exercise and the brain: something to chew on. Trends in neurosciences, 32: 283–290.
[21] Villers, A., Godaux, E., Ris, L. (2012). Long-lasting LTP requires neither repeated trains for its induction nor protein synthesis for its development. PloS one, 7: e40823.
[44] Wang, D., Cui, Z., Zeng, Q., Kuang, H., Wang, L. P., Tsien, J. Z., Cao, X. (2009). Genetic enhancement of memory and long-term potentiation but not CA1 long-term depression in NR2B transgenic rats. PloS one, 4: e7486.
[32] Wang, M., Gamo N. J., Yang, Y., Jin, L. E., Wang, X. J., Laubach, M., Mazer, J. A., Lee, D., Arnsten, A. F. (2011). Neuronal basis of age-related working memory decline. Nature, 476: 210–213.
[19] White, N. M., McDonald, R. J. (2002). Multiple parallel memory systems in the brain of the rat. Neurobiology of learning and memory, 77: 125–184.
[64] Williams, G. V., Goldman-Rakic, P. S. (1995). Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature, 376: 572–575.
[31] Xia, M., Huang, R., Guo, V., Southall, N., Cho, M.-H., Inglese, J., Austin, C. P., Nirenberg, M. (2008). Identification of compounds that potentiate CREB signaling as possible enhancers of long-term memory. Proceedings of the National Academy of Sciences, 106: 2412–2417.
[47] Yamamoto, S., Morinobu, S., Fuchikami, M., Kurata, A., Kozuru, T., Yamawaki, S. (2008). Effects of single prolonged stress and D-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD. Neuropsychopharmacology, 33: 2108–2116.
[68] Yang, S-n. (2000). Sustained Enhancement of AMPA Receptor- and NMDA Receptor-Mediated Currents Induced by Dopamine D1 / D5 Receptor Activation in the Hippocampus : An Essential Role of Postsynaptic Calcium. Hippocampus, 10: 57–63.
[70] Yehuda, R. (2002). Post-traumatic stress disorder. The New England Journal of Medicine, 346: 109–114.
[25] Yin, J. C, Del Vecchio, M., Zhou, H., Tully, T. (1995). CREB as a memory modulator: induced expression of adCREB2 activator isoform enhances long-term memory in Drosophila. Cell, 81: 107–115.
[89] Agis-Balboa, R. C., Arcos-Diaz, D., Wittnam, J., Govindarajan, N., Blom, K., Burkhardt, S., Haladyniak, U., Agbemenyah, H. Y., Zovoilis, A., Salinas-Riester, G., et al. (2011). A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. The EMBO journal, 30: 4071–4083.
[22] Alberini, C. M. (2008). The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol Learn Mem, 89: 234–246.
[1] Alberini, C. M. (2009). Transcription Factors in Long-Term Memory and Synaptic Plasticity. Physiolological Reviews, 89: 121–145.
[28] Alberini, C. M. (2012). Chen DY. Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends in neurosciences, 35: 274–283.
[97] Alberini, C. M., Milekic, M. H., Tronel, S. (2006). Mechanisms of memory stabilization and de-stabilization. Cellular and molecular life sciences, 63: 999–1008.
[81] Azari, N. P. (1991). Psychopharmacology Effects of glucose on memory processes in young adults. Psychopharmacology, 105: 521–524.
[37] Barco, A., Pittenger, C., Kandel, E. R. (2003). CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert opinion on therapeutic targets, 7: 101–114.
[24] Bartsch, D., Ghirardi, M., Skehel, P.A., Karl, K. A., Herder, S. P., Chen, M., Bailey, C. H., Kandel, E. R. (1995). Aplysia CREB2 Represses Long-Term Facilitation: Relief of Repression Converts Transient Facilitation into Long-Term Functional and Structural Change. Cell, 83: 979–992.
[95] Bekinschtein, P., Cammarota, M., Igaz, L. M., Bevilaqua, L. R., Izquierdo, I., Medina, J. H. (2007). Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus. Neuron, 53: 261–277.
[86] Benedict, C., Hallschmid, M., Hatke, A., Schultes, B., Fehm, H. L., Born, J., Kern, W. (2004). Intranasal insulin improves memory in humans. Psychoneuroendocrinology, 29: 1326–1334.
[78] Birks, J. (2009). Cholinesterase inhibitors for Alzheimer’s disease (Review). The Cochrane Library.
[2] Bliss, T. V. P., Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361: 31–39.
[60] Bourne, J., Harris, K. M. (2007). Do thin spines learn to be mushroom spines that remember? Current opinion in neurobiology, 17: 381–386.
[27] Brightwell, J. J., Smith, Ca., Neve, R. L., Colombo, P. J. (2007). Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learning &memory, 14: 195–199.
[45] Burgdorf, J., Zhang, X.-l., Weiss, C., Matthews, E., Disterhoft, J. F., Stanton, P. K., Moskal, J. R. (2011). The Nmethyl-D-aspartate receptor modulator GLYX-13 enhances learning and memory in young adult and learning impaired aged rats. Neurobiology of aging, 21: 698–706.
[59] Cambon, K., Hansen, S. M., Venero, C., Herrero, aI., Skibo, G., Berezin, V., Bock, E., Sandi, C. (2004). A synthetic neural cell adhesion molecule mimetic peptide promotes synaptogenesis, enhances presynaptic function, and facilitates memory consolidation. The Journal of neuroscience, 24: 4197–4204.
[15] Cansino, S. (2009). Episodic memory decay along the adult lifespan: a review of behavioral and neurophysiological evidence. Int J Psychophysiol, 71: 64–69.
[12] Carlesimo, G. A, Oscar-Berman, M. (1992). Memory deficits in Alzheimer's patients: a comprehensive review. Neuropsychol Rev, 3: 119–169.
[65] Castner, Sa., Goldman-Rakic, P. S. (2004). Enhancement of working memory in aged monkeys by a sensitizing regimen of dopamine D1 receptor stimulation. The Journal of neuroscience, 24: 1446–1450.
[30] Chen, A., Muzzio, Ia., Malleret, G., Bartsch, D., Verbitsky, M., Pavlidis, P., Yonan, A. L., Vronskaya, S., Grody, M. B., Cepeda, I., et al. (2003). Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins. Neuron, 39: 655–669.
[36] Chen, D. Y., Stern, Sa., Garcia-Osta, A., Saunier-Rebori, B., Pollonini, G., Bambah-Mukku, D., Blitzer, R. D., Alberini, C. M. (2011). A critical role for IGF-II in memory consolidation and enhancement. Nature, 469: 491–497.
[5] Cooke, S. F, Bliss, T. V. P. (2003). Cellular and Molecular Life Sciences Visions & Reflections The genetic enhancement of memory. Neuropharmacology, 60: 1–5.
[18] Corkin, S, Amaral, D. G., Gonzalez, R. G., Johnson, K. A. (1997). Hyman BTHM's medial temporal lobe lesion: findings from magnetic resonance imaging. J Neurosci, 17: 3964–3979.
[7] Cowan, N. (2008). What are the differences between long-term, short-term, and working memory? Prog Brain Res, 169: 323–338.
[87] Craft, S., Asthana, S., Newcomer, J. W., Wilkinson, C. W., Matos, I. T., Baker, L. D., Cherrier, M., Lofgreen, C., Latendresse, S., Petrova, A., et al. (1999). Enhancement of memory in Alzheimer disease with insulin and somatostatin, but not glucose. Archives of general psychiatry, 56: 1135–1140.
[88] Craft, S., Baker, L. D., Montine, T. J., Minoshima, S., Watson, G. S., Claxton, A., Arbuckle, M., Callaghan, M., Tsai, E., Plymate, S. R., et al. (2012). Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Archives of neurology, 69: 29–38.
[40] Cui, Y., Jin, J., Zhang, X., Xu, H., Yang, L., Du, D., Zeng, Q., Tsien, J. Z., Yu, H., Cao, X. (2011). Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PloS one, 6: e20312.
[42] Danysz, W., Zajaczkowski, W., Parsons, C. G. (1995). Modulation of leaning processes by ionotropic glutamate receptor ligands. Behavioral Pharmacology, 6: 455–474.
[20] Davis, H. P, Squire, L. R. (1984). Protein synthesis and memory: a review. Psychological bulletin, 96: 518–559.
[100] Dębiec, J., Bush, DEa., LeDoux, J. E. (2011). Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats--a possible mechanism for the persistence of traumatic memories in PTSD. Depression and anxiety, 28: 186–193.
[77] Deiana, S., Platt, B., Riedel, G. (2011). The cholinergic system and spatial learning. Behavioural brain research, 221: 389–411.
[67] de Lima, M. N. M., Presti-Torres, J., Dornelles, A., Scalco, F. S., Roesler, R., Garcia, V. A., Schröder, N. (2011). Modulatory influence of dopamine receptors on consolidation of object recognition memory. Neurobiology of learning and memory, 95: 305–310.
[58] Diana, G., Valentini, G., Travaglione, S., Falzano, L., Pieri, M., Zona, C., Meschini, S., Fabbri, A., Fiorentini, C. (2007). Enhancement of learning and memory after activation of cerebral Rho GTPases. Proceedings of the National Academy of Sciences, 104: 636–641.
[14] Dubois, B., Pillon, B. (1997). Cognitive deficits in Parkinson’s disease. Journal of Neurology, 244: 2–8.
[6] Ebbinghaus, H. (1913). Memory: A contribution to experimental psychology. Teachers College, Columbia University.
[51] Ehlers, M. D. (2000). Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron, 28: 511–525.
[71] Eich, T. S., Metcalfe, J. (2009). Effects of the stress of marathon running on implicit and explicit memory. Psychonomic bulletin & review, 16: 475–479.
[62] Floresco, S. B. (2011), Jentsch JD. Pharmacological enhancement of memory and executive functioning in laboratory animals. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology, 36: 227–250.
[82] Foster, J. K., Lidder, P. G., Sünram, S. I. (1998) Glucose and memory: fractionation of enhancement effects? Psychopharmacology, 137: 259–270.
[73] Gold, P. E., Ruskirk, R. V. A. N. (1976). Effects of Posttrial Hormone Injections on Memory Processed. Hormones and Behavior, 7: 509–517.
[84] Gold, P. E., Vogt, J., Hall, J. L. (1986). Glucose effects on memory: behavioral and pharmacological characteristics. Behavioral and neural biology, 46: 145–155.
[91] Hawkes, C., Jhamandas, J. H., Harris, K. H., Fu, W., MacDonald, R. G., Kar, S. (2006). Single transmembrane domain insulin-like growth factor-II/mannose-6-phosphate receptor regulates central cholinergic function by activating a G-protein-sensitive, protein kinase C-dependent pathway. The Journal of neuroscience: the official journal of the Society for Neuroscience, 26: 585–596.
[66] Haycock, J. W., Van Buskirk, R., Ryan, J. R., McGaugh, J. L. (1977). Enhancement of retention with centrally administered catecholamines. Experimental neurology, 54: 199–208.
[54] Hu, H., Real, E., Takamiya, K., Kang, M.-G., Ledoux, J., Huganir, R. L., Malinow, R. (2007). Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell, 131: 160–173.
[99] Inda, M. C., Muravieva, E. V., Alberini, C. M. (2011). Memory retrieval and the passage of time: from reconsolidation and strengthening to extinction. The Journal of neuroscience: the official journal of the Society for Neuroscience, 31: 1635–1643.
[43] Izquierdo, I. (1994). Pharmacological in memory evidence for a role of long-term potentiation. The FASEB Journal, 8: 1139–1145.
[26] Josselyn, Sa., Shi, C., Carlezon, Wa, Neve, R. L., Nestler, E. J., Davis, M. (2001). Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. The Journal of neuroscience, 21: 2404–2412.
[46] Kalisch, R., Holt, B., Petrovic, P., De Martino, B., Klöppel, S., Büchel, C., Dolan, R. J. (2009). The NMDA agonist D-cycloserine facilitates fear memory consolidation in humans. Cerebral cortex, 19: 187–196.
[55] Krugers, H. J., Hoogenraad, C. C., Groc, L. (2010). Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nature reviews. Neuroscience, 11: 675–681.
[61] Kupfermann, I. (1979). Modulatory actions of neurotransmitters. Annual review of neuroscience, 2: 447–465.
[38] Lamprecht, R., LeDoux, J. (2004). Structural plasticity and memory. Nature reviews. Neuroscience, 5: 45–54.
[80] Lapp, J. E. (1981). Effects of Glycemic Alterations and Noun Imagery on the Learning of Paired Associates. Journal of Learning Disabilities, 14: 35–38.
[29] Lee, J.-A., Kim, H., Kim, K., Han, J. (2001). Overexpression of and RNA interference with the CCAAT enhancer-binding protein on long-term facilitation of Aplysia sensory to motor synapses. Learning and Memory, 8: 220–226.
[4] Lee, Y-S, Silva, A. J. (2009). The molecular and cellular biology of enhanced cognition. Nature reviews. Neuroscience, 10: 126–140.
[102] Leuner, B., Shors, T. J. (2004). New spines, new memories. Mol Neurobiol, 29: 117–130.
[16] Light, L. L. (1991). Memory and aging: four hypotheses in search of data. Annu Rev Psychol, 42: 333–376.
[75] Linssen, aM. W., Vuurman, E. F. P. M., Sambeth, A., Riedel, W. J. (2011). Methylphenidate produces selective enhancement of declarative memory consolidation in healthy volunteers. Psychopharmacology.
[93] Lynch, G. (2002). Memory enhancement: the search for mechanism-based drugs. Nature neuroscience, 5(Suppl): 1035–1038.
[52] Lynch, G. (2006). Glutamate-based therapeutic approaches: ampakines. Current opinion in pharmacology, 6: 82–88.
[10] Lynch, G, Palmer, L.C., Gall, C. M. (2011). The likelihood of cognitive enhancement. Pharmacology, biochemistry, and behavior, 99: 116–129.
[33] Malleret, G., Haditsch, U., Genoux, D., Jones, M. W., Bliss, T. V., Vanhoose, aM., Weitlauf, C., Kandel, E. R., Winder, D. G., Mansuy, I. M. (2001). Inducible and reversible enhancement of learning, memory, and longterm potentiation by genetic inhibition of calcineurin. Cell, 104: 675–686.
[8] McGaugh, J. L. (2000). Memory - A Century of Consolidation. Science, 287: 248–251.
[9] Nader, K, Einarsson, E. O. (2010). Memory reconsolidation: an update. Ann N Y Acad Sci, 1191: 27–41.
[69] McGaugh, J. L., Roozendaal, B. (2002). Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology, 12: 205–210.
[63] Mckeith, I. G., Burn, D. (2000). Spectrum of Parkinson's Disease, Parkinson's Dementia, and Lewy Body Dementia. Neurologic Clinics, 18: 865–883.
[85] McNay, E. C., Ong, C. T., McCrimmon, R. J., Cresswell, J., Bogan, J. S., Sherwin, R. S. (2010). Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiology of learning and memory, 93: 546–553.
[56] McReynolds, J. R., Donowho, K., Abdi, A., McGaugh, J. L., Roozendaal, B., McIntyre, C.K. (2010). Memoryenhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiology of learning and memory, 93: 312–321.
[49] Migues, P. V., Hardt, O., Wu, D. C., Gamache, K., Sacktor, T. C., Wang, Y. T., Nader, K. (2010). PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nature neuroscience, 13: 630–634.
[103] Mizuno, K., Giese, K. P. (2010). Towards a molecular understanding of sex differences in memory formation. Trends Neurosci, 33: 285–291.
[57] Okuno, H., Akashi, K., Ishii, Y., Yagishita-Kyo, N., Suzuki, K., Nonaka, M., Kawashima, T., Fujii, H., Takemoto-Kimura, S., Abe, M., et al. (2012). Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIbeta. Cell, 149: 886–898.
[13] Perry, R. J., Hodges, J. R. (1999). Attention and executive deficits in Alzheimer’s disease A critical review. Brain, 122: 383–404.
[96] Pinsker, H. M, Hening, W. A., Carew, T. J., Kandel, E. R. (1973). Long-term sensitization of a defensive withdrawal reflex in Aplysia. Science, 182: 1039–1042.
[79] Prickaerts, J., Sik, A., van der Staay, F. J., de Vente, J., Blokland, A. (2005). Dissociable effects of acetylcholinesterase inhibitors and phosphodiesterase type 5 inhibitors on object recognition memory: acquisition versus consolidation. Psychopharmacology, 177: 381–390.
[48] Rao, V. R., Finkbeiner, S. (2007). NMDA and AMPA receptors: old channels, new tricks. Trends in Neurosciences, 30: 284–291.
[92] Reinhardt, R. R., Bondy, C. A. (1994). Insulin-Like Growth Factors Cross the Blood-Brain Barrier. Endocrinology, 135: 1753–1761.
[3] Ressler, K. J., Mayberg, H. S. (2007). Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nature neuroscience, 10: 1116–1124.
[41] Riedel, G., Platt, B., Micheau, J. (2003). Glutamate receptor function in learning and memory. Behavioural brain research, 140: 1–47.
[74] Roozendaal, B., Nguyen, B. T., Power, A. E., Mcgaugh, J. L. (1999). Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proceedings of the National Academy of Sciences, 96: 11642–11647.
[72] Roozendaal, B., Okuda, S., Van der Zee, Ea., McGaugh, J.L. (2006). Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences, 103: 6741–6746.
[90] Roth, Ra. (1988). Structure of the receptor for insulin-like growth factor II: the puzzle amplified. Science, 239: 1269–1271.
[98] Sara, S. J. (2000). Strengthening the shaky trace through retrieval. Nature reviews. Neuroscience, 1: 212–213.
[34] Sharma, S. K., Bagnall, M. W., Sutton, Ma., Carew, T. J. (2003). Inhibition of calcineurin facilitates the induction of memory for sensitization in Aplysia: requirement of mitogen-activated protein kinase. Proceedings of the National Academy of Sciences of the United States of America, 100: 4861–4866.
[23] Sharma, A. V., Nargang, F. E., Dickson, C.T. (2012). Neurosilence: profound suppression of neural activity following intracerebral administration of the protein synthesis inhibitor anisomycin. J Neurosci, 32: 2377–2387.
[50] Shema, R., Haramati, S., Ron, S., Hazvi, S., Chen, A., Sacktor, T. C., Dudai, Y. (2011). Enhancement of consolidated long-term memory by overexpression of protein kinase Mzeta in the neocortex. Science, 331: 1207–1210.
[11] Simard, M, Reekum, R. V. (1999). Memory Assessment in Studies of Cognition-Enhancing Drugs for Alzheimer’s Disease. Drugs and Aging, 14: 197–230.
[53] Slutsky, I., Abumaria, N., Wu, L.-J., Huang, C., Zhang, L., Li, B., Zhao, X., Govindarajan, A., Zhao, M.-G., Zhuo, M., et al. (2010). Enhancement of learning and memory by elevating brain magnesium. Neuron, 65: 165–177.
[83] Smith, Ma, Riby, L. M., Eekelen, J. A. M. V., Foster, J. K. (2011). Glucose enhancement of human memory: a comprehensive research review of the glucose memory facilitation effect. Neuroscience and biobehavioral reviews, 35: 770–783.
[17] Squire, L. R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological review, 99: 195–231.
[39] Tang, Y. P., Shimizu, E., Dube, G. R., Rampon, C., Kerchner, Ga., Zhuo, M., Liu, G., Tsien, J. Z. (1999). Genetic enhancement of learning and memory in mice. Nature, 401: 63–69.
[101] Tian, S., Huang, F., Li, P., Li, Z., Zhou, S., Deng, H., Yang, Y. (2011). Nicotine enhances contextual fear memory reconsolidation in rats. Neuroscience letters, 487: 368–371.
[35] Tully, T., Bourtchouladze, R., Scott, R., Tallman, J. (2003). Targeting the CREB pathway for memory enhancers. Nature reviews. Drug discovery, 2: 267–277.
[94] van Praag, H. (2009). Exercise and the brain: something to chew on. Trends in neurosciences, 32: 283–290.
[21] Villers, A., Godaux, E., Ris, L. (2012). Long-lasting LTP requires neither repeated trains for its induction nor protein synthesis for its development. PloS one, 7: e40823.
[44] Wang, D., Cui, Z., Zeng, Q., Kuang, H., Wang, L. P., Tsien, J. Z., Cao, X. (2009). Genetic enhancement of memory and long-term potentiation but not CA1 long-term depression in NR2B transgenic rats. PloS one, 4: e7486.
[32] Wang, M., Gamo N. J., Yang, Y., Jin, L. E., Wang, X. J., Laubach, M., Mazer, J. A., Lee, D., Arnsten, A. F. (2011). Neuronal basis of age-related working memory decline. Nature, 476: 210–213.
[19] White, N. M., McDonald, R. J. (2002). Multiple parallel memory systems in the brain of the rat. Neurobiology of learning and memory, 77: 125–184.
[64] Williams, G. V., Goldman-Rakic, P. S. (1995). Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature, 376: 572–575.
[31] Xia, M., Huang, R., Guo, V., Southall, N., Cho, M.-H., Inglese, J., Austin, C. P., Nirenberg, M. (2008). Identification of compounds that potentiate CREB signaling as possible enhancers of long-term memory. Proceedings of the National Academy of Sciences, 106: 2412–2417.
[47] Yamamoto, S., Morinobu, S., Fuchikami, M., Kurata, A., Kozuru, T., Yamawaki, S. (2008). Effects of single prolonged stress and D-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD. Neuropsychopharmacology, 33: 2108–2116.
[68] Yang, S-n. (2000). Sustained Enhancement of AMPA Receptor- and NMDA Receptor-Mediated Currents Induced by Dopamine D1 / D5 Receptor Activation in the Hippocampus : An Essential Role of Postsynaptic Calcium. Hippocampus, 10: 57–63.
[70] Yehuda, R. (2002). Post-traumatic stress disorder. The New England Journal of Medicine, 346: 109–114.
[25] Yin, J. C, Del Vecchio, M., Zhou, H., Tully, T. (1995). CREB as a memory modulator: induced expression of adCREB2 activator isoform enhances long-term memory in Drosophila. Cell, 81: 107–115.
Published
2020-12-17
How to Cite
Alberini, C., & STERN, S. (2020). Mechanisms of Memory Enhancement. Critical Hermeneutics, 4(special II), 121-166. https://doi.org/10.13125/CH/4495
Issue
Section
Articles
Copyright (c) 2020 Cristina M. Alberini, SARAH A. STERN
Copyrights for articles published in Critical Hermeneutics are retained by the authors, with first publication rights granted to the journal.
Critical Hermeneutics is published under a Creative Commons Attribution Licence CC BY 3.0
. With the licence CC-BY, authors retain the copyright, allowing anyone to download, reuse, re-print, modify, distribute and/or copy the contribution (edited version), on condition that credit is properly attributed to its author and that Critical Hermeneutics is mentioned as its first venue of publication.
